A Hidden Markov Model reveals magnetoencephalography spectral frequency-specific abnormalities of brain state power and phase-coupling in neuropathic pain

Abstract

Neuronal populations in the brain are engaged in a temporally coordinated manner at rest. Here we show that spontaneous transitions between large-scale resting-state networks are altered in chronic neuropathic pain. We applied an approach based on the Hidden Markov Model to magnetoencephalography data to describe how the brain moves from one activity state to another. This identified 12 fast transient (~80 ms) brain states including the sensorimotor, ascending nociceptive pathway, salience, visual, and default mode networks. Compared to healthy controls, we found that people with neuropathic pain exhibited abnormal alpha power in the right ascending nociceptive pathway state, but higher power and coherence in the sensorimotor network state in the beta band, and shorter time intervals between visits of the sensorimotor network, indicating more active time in this state. Conversely, the neuropathic pain group showed lower coherence and spent less time in the frontal attentional state. Therefore, this study reveals a temporal imbalance and dysregulation of spectral frequency-specific brain microstates in patients with neuropathic pain. These findings can potentially impact the development of a mechanism-based therapeutic approach by identifying brain targets to stimulate using neuromodulation to modify abnormal activity and to restore effective neuronal synchrony between brain states.

Connectivity-based Meta-Bands: A new approach for automatic frequency band identification in connectivity analyses

“…This association with the posterior DMN is supported by previous studies which found that these areas were strongly active [91,92], and highly connected [92] in the alpha frequencies during rest. Interestingly, the posterior areas of the DMN have been associated with higher cognitive functions such as the integration of information, attention, empathy, self-consciousness mental thoughts that occur during rest, and theory of mind [93,89,91].…”

“…A similar beta-band network topology has been observed in a previous study using MEG resting-state recordings [88]. Although this association is not as clear as for the blue meta-state, this topology could be associated with the anterior areas of the DMN [91,92]. This network has been observed to be highly active for low frequencies (around theta), but not in beta [91,92].…”

“…This occipital topology could be related to the posterior areas of the default-mode network (DMN), which has been proposed to be the dominant brain activity during rest. Some studies have suggested that the DMN consist of two subnetworks: anterior DMN, and posterior DMN [89,90,91,92]. This association with the posterior DMN is supported by previous studies which found that these areas were strongly active [91,92], and highly connected [92] in the alpha frequencies during rest.…”

“…Although this association is not as clear as for the blue meta-state, this topology could be associated with the anterior areas of the DMN [91,92]. This network has been observed to be highly active for low frequencies (around theta), but not in beta [91,92]. The anterior areas of the DMN are involved in high cognitive functions such as semantic integration, emotions, and decision making [94,95].…”

“…The anterior areas of the DMN are involved in high cognitive functions such as semantic integration, emotions, and decision making [94,95]. The beta frequency activation of this meta-band may be related with the sensorimotor network, which has been reported to be very active and connected around beta frequencies, and displays a topology with some areas overlapping with the brown meta-band [91]. This network is also highly reported in intrinsic neural activity, and is involved in perception, proprioception, and motion [96,97,98].…”